Hard-to-Please Females May Be Neglected Evolutionary Force

By NATALIE ANGIER

Published: May 8, 1990

WHAT do females want? Every man who has ever rolled his eyes heavenward in apparent bafflement at this great enigma might do well to follow the example of evolutionary biologists: stop speculating and start paying attention to the evidence at hand.

In laboratories and field research stations across the United States and abroad, biologists are analyzing an evolutionary force that has long been neglected: the effect of female choice on the appearance and performance of males.

The new results indicate that many of the mysterious and seemingly irrelevant courtship rituals and male displays in the animal kingdom serve a crucial purpose of allowing a female to judge the robustness or health of her potential mate before committing herself to the union.

Biologists have suspected for years that certain flamboyant features among males, like the peacock's Technicolor tail and the bullfrog's booming moonlight sonatas, evolved for no other purpose than to allow males to curry favor with females. But many researchers dismissed the role of female choice as a minor influence in evolution of animal traits compared with the ability to elude predators or defend territory, or with war-like competition among males for access to mates.

Now the female animal is finally coming into her own in the biological arena. Galvanized by new research tools and more sophisticated evolutionary theories, biologists are designing experiments to measure precisely the features that entice females to mate with one male rather than another.

Through elaborate statistical analyses and, in some cases, laboratory manipulations, biologists who study courtship in animals are replacing what Harvard biologist Stephen Jay Gould has called ''Just So stories'' - the old Aesop animal fables - with rigorous data.

''We're trying to do experimental work where we manipulate characteristics, to see how changing these traits changes what the female does,'' said Marlene Zuk, a biologist at the University of California at Riverside. ''In that way we can begin teasing apart what a female is actually choosing, not just what we think makes good sense for her to be choosing.''

The latest findings, published in recent issues of Nature and presented at several international meetings, suggest that females of many species pay particularly close attention to telltale signs of parasitism or disease. As a result, the males often sport skin colorations or feather patterns to signal robust health, which then become accentuated or exaggerated over generations of selection by females.

Some female birds and frogs demand of their suitors in courtship a performance that pushes the males to their cardiovascular limits, perhaps as a test of the hardiness of the males' genes.

In other species, especially insects, a female will refuse a male's sexual overtures unless he offers her some sort of nuptial gift, usually a defensive chemical that she can use to protect herself or her eggs.

The long-term consequences of female choice affect the characteristics of females as well as of their mates, scientists say; daughters presumably inherit from their mothers a predisposition to favor certain masculine traits over others.

Finding Subtle Dynamics

Biologists emphasize that they are just beginning to understand the complex dynamics of female choice, and that the whys and wherefores of female taste remain elusive for the great majority of species. ''Female choice is more subtle than something like male-male competition, because it affects not only the evolution of the male, but of female preference,'' said Dr. Mark Kirkpatrick, a zoologist at the University of Texas in Austin. Nevertheless, he added, ''it's definitely the wave of the future in biology.'' Theory Slighted for a Century Charles Darwin proposed in 1872 that female animals could exert pressure on the evolution of their species in their mating decisions, but the theory was largely slighted for almost a century. It began its comeback in the mid-1970's, when biologists turned away from studies of amorphous group behavior among animals and instead focused on the actions and reproductive strategies of individuals in a species.

Fleshing out the ideas of Darwin and other pioneering naturalists, animal behaviorists proposed that females usually have a larger stake in reproduction than males do. The stake is especially high in female mammals that bear their young and then care for the offspring after birth. But even for insects and fish, which invest far less time in rearing young, the amount of energy needed to produce the nutrients, fat and protein of an egg is greater than that required for generating sperm.

''Eggs are expensive,'' said Dr. Thomas Eisner, an evolutionary biologist at Cornell University. ''Sperm is cheap.''

Given their greater investment in reproduction, say biologists, females have greater incentive than males to seek the best possible mate. Males that want to pass their legacy to future generations must either appeal to females, or suffer a genetic dead end.

Perhaps the most straightforward work on the fine points of female finickiness has come in species where the female seeks material help from the male in the rearing or protection of the young.

Role of One Chemical for Beetles

In ongoing investigations of the courtship behavior of a beetle species called Pyrochroidae, Dr. Eisner, Dr. Jerrold Meinwald and their colleagues have determined why the male beetle goes through the peculiar ritual of displaying to a potential mate a deep cleft in his forehead. The researchers have found that stashed within the cleft is a small dose of the chemical cantharidin, familiarly known as Spanish fly.

The source of the male beetle's cantharidin is still mysterious, though Dr. Eisner suspects that it comes from eating the eggs of another insect, the blister beetle. During courtship, the male exposes his cleft to the female, she grabs his head and immediately laps up the chemical offering. Apparently placated, she allows the male to mate.

The Cornell scientists have determined that the male transfers to the female a much larger quantity of cantharidin during intercourse, and that she subsequently incorporates the chemical into her eggs, which thenceforth are protected against ants and other common predators of beetle eggs.

''The male gives her a little teaser during foreplay,'' said Dr. Eisner. ''It's as though he's showing her a fat wallet and saying, 'There's more in the bank where that came from.' ''

To prove the central importance of cantharidin, the scientists raised male beetles in the lab, where they had no access to the chemical. True to the theory, the cantharidin-free males failed dismally at mating. ''Ninety percent of the males with cantharidin eventually manage to mate, but less than 20 percent of the cantharidin-free males succeed,'' said Dr. Eisner. ''Only the ones that literally rape-mount the female get anywhere at all.''Choosing From Appearance Less obvious than a nuptial gift is what a female seeks when she chooses on the basis of a male's appearance. In an experiment described in a recent issue of Nature, scientists from the University of Bern in Switzerland examined the impact of a male's coloration on female choice among the three-spined stickleback, a small fish.

The researchers knew that in breeding season, the male stickleback turns a bright red and upon changing color, it displays itself before a female in a mating dance of zigs and zags. The biologists also knew that males exposed to parasites turned a dimmer shade of red, even afer shaking off the parasitic disease. Their question: Did females prefer males that possessed the bright red color signaling current and prior health?

To address the problem, they tested female responsiveness to groups of brilliant red males and dimmer, previously parasitized males under natural white light, in which the females could see the intensity of the red color, and under green light, which disguised the relative tones.

The scientists found that when females could distinguish red males from their drearier counterparts, the females almost uniformly paired up with the brighter males, although both groups of suitors performed the zigzag courtship dance with equal zest.

Dr. Zuk believes that female birds also are preoccupied with parasites. In experiments with red jungle fowl, the ancestors of barnyard chickens, she and Dr. Randy Thornhill and Dr. David Ligon, biologists at the University of New Mexico in Albuquerque, identified the specific ornaments that most attracted a hen to a rooster. The biologists found that hens paid closer attention to the condition of the male's comb and wattle than to any other characteristic, including size, weight, the aggressiveness of his strutting, or the state of his feathers.

Stamina Also a Factor

The longer the comb and the brighter the wattle, the more likely the hen was to choose him over a competing rooster. As it turns out, combs and wattles are also the traits by which farmers judge the health of their flock.

''The females didn't seem to care how big the rooster was, or whether his feathers were smooth,'' said Dr. Zuk. ''It's the fleshy parts, the wattle, the comb color and size, that can change in a matter of days depending on parasitism, and that's what the hen seemed to be looking at.''

Beyond resistance to disease, another factor that females seem to find alluring is stamina. Dr. H. Carl Gerhardt, a biologist at the University of Missouri in Columbia, has analyzed the calls of gray tree frogs. Male frogs sit for days attempting to attract females by repeating a series of trilling pulses that they can vary in both length of individual pulses and timing between pulses.

Studying the physiology of the calls, Dr. Gerhardt and his colleagues discovered that male frogs consume an extraordinary amount of oxygen and deplete their body's fuel rations to generate their croons. ''It's energetically demanding,'' he explains. ''The frog reaches the same metabolic rate during calling that you get by forcing him to exercise to exhaustion. It's as though the female was asking him to push against his physiological limit.''

Dr. Gerhardt also has used electronic frog calls in an attempt to determine if females are drawn to artificial sounds that exceed the calling capacity of the hardiest real frog. Generating synthetic pulses through one speaker at a normal song rate and through another at twice that rate, the team has found that female frogs leap wildly in the direction of the fast-trilling speakers, sometimes attempting to embrace the singing machine.

Other species of frog also prefer the most athletic callers, said Dr. Gerhardt. In this way, he suggested, ''thefemales assure that they avoid the obvious wimps.''

Because a male tree frog contributes nothing to the business of reproduction beyond his genes - no defensive chemicals and no caring for the young - a female selecting a male for stamina presumably hopes to gain from the exchange the probability of begetting vigorous young.

Long Tails Chosen by Females

But proving that hardy males sire hardy offspring has been difficult and the subject of great contention among biologists. Some of the strongest evidence supporting the link has come lately from Dr. Anders Moller, a biologist at the University of Uppsala in Sweden. He has studied barn swallows, in which the males have tails that are about 20 percent longer than those of the female.

Dr. Moller first determined that female choice had determined the long tails of the male. He cut feathers off the tails of some male birds, and glued extra feathers to the tails of others.

When permitted to choose between the short-tails and the long-tails, the females invariably selected the more amply endowed males.

Dr. Moller next investigated possible reasons for the female preference. Like other researchers, he found a link between the chosen males and resistance to parasites. The longer-tailed males had measurably fewer blood-sucking mites on their bodies than did the short-tails.

To investigate whether the long-tailed birds had some sort of genetic resistance to the mites the biologist decided to follow the swallows through several generations. More significantly, he switched the eggs that had been fertilized by long-tailed males with those spawned by shorter-tailed males, to offset the contributions of environmental factors.

After making the switches, he infected the nests of all the birds with the same number of mites. Dr. Moller found that, as they grew, young birds of either sex sired by the long-tailed males had significantly fewer parasites on their bodies than did the offspring of short-tailed males.

The chicks' resistance to mites had no correlation to which nest they were in, or to the number of parasites crawling across their foster parents' feathers, but rather was determined by the relative parasite load on the natural father, a strong indication that resistance is hereditary.

Why long tails and resistance correspond remains mysterious, but a female actively chooses the longest-tailed mate around, apparently in an effort to bequeath to her young the best possible genetic legacy.

''About 15 percent of males never seem to get the chance to mate,'' he said. ''And they are almost always the males with the shortest tails.''

Biologists warn that what is true for barn swallows may not turn out to be true for other animals. Many of them believe that many cases of female choice will prove to be somewhat arbitrary - that a female pairs up with an especially loud male, for example, just because he is the one she hears.

''The ultimate question always is, does the female really get anything out of the choice she makes?'' said Robert Gibson, a biologist at the University of California at Los Angeles who studies female choice in the sage grouse. ''Is she really making a choice, or does it just seem that way to us? In so many cases, we still don't know.''

Choosy Female Seeks Robust Mate

When females judge male markings, songs and other mating displays, they may not just be looking for another handsome face. Some biologists say the signs the females look for demonstrate the male's fitness as a father. In wild chickens, for example, a long comb and bright wattle signify a rooster free of parasites. The male tree frog's trilling song needs large pulses of oxygen; a loud serenade proves the male is strong and vigorous. The male pyrochroidae beetle is less subtle. He displays in a forehead cleft a chemical that repels predators. If a female allows him to mate, he gives her a supply of the chemical for her eggs.